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Page 1: Phenotypic plasticity in plants

Plant Species Biology (2002) 17, 85–88

© 2002 The Society for the Study of Species Biology

Blackwell Science, LtdOxford, UKPSBPlant Species Biology1441 0745The Society for the Study of Species Biology, 2002

17

2 & 3December 2002

083PHENOTYPIC PLASTICITY IN PLANTS

C. D. SCHLICHTING10.1046/j.1441 0745.2002.00083.x

EditorialBEES SGML

Correspondence: Carl D. Schlichting, Ecology & EvolutionaryBiology, University of Connecticut, Storrs CT 06269-3043, USA.Email: [email protected]

Phenotypic plasticity in plants

CARL D. SCHLICHTING

Ecology & Evolutionary Biology, University of Connecticut, Storrs CT 06269-3043, USA.

Introduction

In the 1970s and 1980s, evolutionary biologists were fix-ated on cataloging purely genetic variation—at first withisozymes, then with any other suitable acronym (RAPD,RFLP, VNTR . . . ), and finally with h

2

(heritability). Itseemed at times as though the phenotype itself was oflittle importance. However, those workers who did notforget that, in fact, it is the phenotype that naturalselection ‘sees’, continued to study the other source ofphenotypic variation, the environment. By the 1990s,the pendulum started shifting back towards a morebalanced perspective, with an increased appreciation thatthe phenotype is molded by an interplay of genetic andenvironmental effects.

I suspect that the study of phenotypic plasticity playedan important part in that reversal, and botanical research-ers led the way (top two in citations per year before 1994,Table 1). In fact, the study of plasticity has continued toexpand rapidly in the last decade. A scan of the citationdatabase

Web of Science

shows that the number of papersusing the phrase

phenotypic plasticity

has steadilyincreased from 138 (per million documents) to 167 and225 (in 1994, 1998 and halfway through 2002, respec-tively).

In addition to in depth studies of the usual abiotic sus-pects—that is, light, temperature, water and nutrients(e.g. Stuefer

et al

. 1996; Weinig 2000; Lankinen 2001;Meyre

et al

. 2001; Wahl

et al

. 2001)—now studies routinelygo beyond to investigate biotic environmental influenceson the phenotype including the roles of competitors,predators and pollinators (e.g. Vogler

et al

. 1998; Fornoni& Núñez-Farfán 2000; Imbert & Ronce 2001; Van Dam &Baldwin 2001). Studies have also become increasinglysophisticated in examining the adaptive nature of plasticresponses (Schmitt

et al

. 1995; Tucic

et al

. 1998; Winn 1999;Clauss & Venable 2000; Donohue

et al

. 2001; Van Kleunen& Fischer 2001).

The links between gene regulation, physiological mech-anisms and morphological plasticity are also receivingmore scrutiny, as scientists investigate the question ofhow much information plants can extract from the envi-ronment around them (Borland

et al

. 1998; Pedrol

et al

.2000; Emery

et al

. 2001; Grime & Mackey 2002; Forde 2002;Pepper

et al

. 2002; Weinig 2002; Schlichting & Smith 2002).A second catalyst for the increased attention on plastic-

ity, and one which will continue to grow in importance,is the re-emergence of interest in the ecology and evolu-tion of plant development (e.g. Matthies 1990; Jones 1992;Diggle 2002; Diggle 1994; Jones 1995; Pigliucci & Schlich-ting 1995; Gedroc

et al

. 1996; Pigliucci 1997; Pigliucci 1998;Sachs 2002). Phenotypic plasticity clearly has its originsin development and this has led to studies of a variety ofissues that examine the impacts of both external and inter-nal environmental conditions on growth and develop-ment. For example,

How do environmental effects on thematernal plant influence offspring development?

(Schaal &Leverich 1984; Roach & Wulff 1987; Schmid & Dolt 1994;Schmitt 1995; Sills & Nienhuis 1995; Lacey 1996; Sultan1996; Donohue & Schmitt 1998; Munir

et al

. 2000; Agrawal2001) and, do prior fruit and flower production affect thelikelihood of subsequent growth and reproductiveevents? (Stephenson

et al

. 1988; Diggle 1994; Diggle 1997;Avila-Sakar

et al

. 2001).The four papers in this issue take distinctive perspec-

tives on plasticity: all are by researchers interested inexpanding the limits of what we know about how andwhy plasticity evolves. In each case the authors take acloser look at a phenomenon of current interest, and askus to perhaps reevaluate the typical interpretation. Kudoh

et al

. offer a fresh angle on the question of the evolutionof optimal flowering time by examining the role that plantresponse to internal factors may play. Murren examinesphenotypic integration in plants from the perspectives ofenvironmental influences on trait correlations and the rela-tionship between the genotype and phenotype. Poultonand Winn tackle the thorny question of detecting costs ofplasticity, with an empiric investigation of selection onphenotypes and plasticity of

Brassica

plants. Wright andMcConnaughay make the case for clearly distinguishing

Page 2: Phenotypic plasticity in plants

86

C . D . S C H L I C H T I N G

© 2002 The Society for the Study of Species Biology

Plant Species Biology

, 17, 85–88

environmental effects on development from effects thatare related to plant size or developmental stage.

Acknowledgments

I thank Professor Shoichi Kawano for the originalinvitation to bring together these papers, and ProfessorToshihiko Hara,

Plant Species Biology

’s editor, for hispatience in waiting for me to deliver the manuscripts.Finally, I am deeply appreciative of the efforts of theexternal referees: their insightful reviews of the papersmade my job far easier. They will, for obvious reasons,remain anonymous.

References

Agrawal A.A. (2001) Transgenerational consequences of plantresponses to herbivory: an adaptive maternal effect?

AmericanNaturalist

157

: 555–569.Avila-Sakar G., Krupnick G.A. & Stephenson A.G. (2001) Growth

and resource allocation in

Cucurbita pepo

ssp

texana

: Effects offruit removal.

International Journal of Plant Sciences

162

: 1089–1095.

Borland A.M., Técsi L.I., Leegood R.C. & Walker R.P. (1998)Inducibility of crassulacean acid metabolism (CAM) in

Clusia

species; physiological/biochemical characterization andintercellular localization of carboxylation and decarboxyla-tion processes in three species which exhibit different degreesof CAM.

Planta

205

: 342–351.Bradshaw A.D. (1965) Evolutionary significance of phenotypic

plasticity in plants.

Advances in Genetics

13

: 115–155.Caswell H. (1983) Phenotypic plasticity in life-history traits:

demographic effects and evolutionary consequences.

American Zoologist

23

: 35–46.

Clauss M.J. & Venable D.L. (2000) Seed germination in desertannuals: an empirical test of adaptive bet hedging.

AmericanNaturalist

155

: 168–186.Diggle P.K. (1994) The expression of andromonoecy in

Solanumhirtum

(Solanaceae): phenotypic plasticity and ontogeneticcontingency.

American Journal of Botany

81

: 1354–1365.Diggle P.K. (1997) Ontogenetic contingency and floral morphol-

ogy: the effects of architecture and resource limitation.

International Journal of Plant Science

158

: S99–S107.Diggle P.K. (2002) A developmental morphologist’s perspective

on plasticity.

Evolutionary Ecology

16

: 267–283.Dodson S. (1989) Predator-induced reaction norms.

Bioscience

39

:447–452.

Donohue K., Pyle E.H., Messiqua D., Heschel M.S. & Schmitt J.(2001) Adaptive divergence in plasticity in natural popula-tions of

Impatiens capensis and

its consequences for perfor-mance in novel habitats.

Evolution

55

: 692–702.Donohue K. & Schmitt J. (1998) Maternal environmental effects

in plants: adaptive plasticity?

Maternal Effects as Adaptations

(eds Mousseau T.A. & Fox C.W.), pp. 137–158. OxfordUniversity Press, New York.

Emery R.J.N., Pharis R.P., Reid D.M. & Chinnappa C.C. (2001)Stem elongation and gibberellins in alpine and prairieecotypes of

Stellaria longipes

.

Plant Growth Regulation

35

: 17–29.

Forde B.G. (2002) The role of long-distance signalling in plantresponses to nitrate and other nutrients.

Journal of Experimen-tal Botany

53

: 39–43.Fornoni J. & Núñez-Farfán J. (2000) Evolutionary ecology of

Datura stramonium

: Genetic variation and costs for toleranceto defoliation.

Evolution

54

: 789–797.Gedroc J.J., McConnaughay K.D.M. & Coleman J.S. (1996)

Plasticity in root/shoot partitioning: optimal, ontogenetic, orboth?

Functional Ecology

10

: 44–50.Grime J.P., Crick J.C. & Rincon J.E. (1986) The ecological signifi-

cance of plasticity. In:

Plasticity in Plants

(eds Jennings D.H.& Trewavas A.J.), pp. 5–29. Pindar, Scarborough, UK.

Table 1

Phenotypic plasticity review arti-cles with over 100 total citations

Author Year Total CitesCites/yearPre-1994

Cites/year1994 -

Bradshaw A.D.* 1965 872

#

23.5 50.1Schlichting C.D.* 1986 403 20.4 30.6Stearns S.C. 1989 306 17.5 27.8West Eberhard M.J. 1989 313 13.0 30.7Dodson S. 1989 150 10.0 12.9Sultan S.E.* 1987 241 9.5 21.6Harvell C.D. 1990 197 9.0 20.0Smith-Gill S.J. 1983 166 8.7 9.3Caswell H. 1983 121 7.8 5.1Grime J.P.

et al

. 1986 141 7.1 10.7Moran N.A. 1992 114 4.0 12.9Shapiro A.M. 1976 106 3.4 5.8Scheiner S.M. 1993 245 – 27.2Via S.

et al

. 1995 172 – 24.6McNamara J.M. & Houston A.I. 1996 116 – 19.3

*botanical emphasis#Bradshaw’s data are calculated since 1975.

Page 3: Phenotypic plasticity in plants

P H E N O T Y P I C P L A S T I C I T Y I N P L A N T S

87

© 2002 The Society for the Study of Species Biology

Plant Species Biology

, 17, 85–88

Grime J.P. & Mackey J.M.L. (2002) The role of plasticity inresource capture by plants.

Evolutionary Ecology

16

: 299–307.Harvell C.D. (1990) The ecology and evolution of inducible

defenses.

Quarterly Review of Biology

65

: 323–340.Imbert E. & Ronce O. (2001) Phenotypic plasticity for dispersal

ability in the seed heteromorphic

Crepis sancta

(Asteraceae).

Oikos

93

: 126–134.Jones C.S. (1992) Comparative ontogeny of a wild cucurbit and

its derived cultivar.

Evolution

46

: 1827–1847.Jones C.S. (1995) Does shade prolong juvenile development? A

morphological analysis of leaf shape changes in

Cucurbitaargyrosperma

subsp.

sororia

(Cucurbitaceae).

American Journalof Botany

82

: 346–359.Lacey E.P. (1996) Parental effects in

Plantago lanceolata

L. I. agrowth chamber experiment to examine pre- and post-zygotic temperature effects.

Evolution

50

: 865–878.Lankinen A. (2001)

In vitro

pollen competitive ability in

Violatricolor

: temperature and pollen donor effects.

Oecologia

128

:492–498.

Matthies D. (1990) Plasticity of reproductive components at dif-ferent stages of development in the annual plant

Thlaspiarvense

L.

Oecologia

83

: 105–116.McNamara J.M. & Houston A.I. (1996) State-dependent life

histories.

Nature

380

: 215–221.Meyre D., Leonardi A., Brisson G. & Vartanian N. (2001)

Drought-adaptive mechanisms involved in the escape/toler-ance strategies of

Arabidopsis

Landsberg

erecta and

Columbiaecotypes and their F

1

reciprocal progeny.

Journal of Plant Phys-iology

158

: 1145–1152.Moran N.A. (1992) The evolutionary maintenance of alternative

phenotypes.

American Naturalist

139

: 971–989.Munir J., Dorn L.A., Donohue K. & Schmitt J. (2000) The effect

of maternal photoperiod on seasonal dormancy in

Arabidopsisthaliana

.

American Journal of Botany

88

: 1240–1249.Pedrol N., Ramos P. & Reigosa M.J. (2000) Phenotypic plasticity

and acclimation to water deficits in velvet-grass: a long-termgreenhouse experiment. Changes in leaf morphology, photo-synthesis and stress-induced metabolites.

Journal of PlantPhysiology

157

: 383–393.Pepper A.E., Corbett R.W. & Kang N. (2002) Natural variation in

Arabidopsis

seedling photomorphogenesis reveals a likely rolefor

TED1

in phytochrome signalling.

Plant Cell and Environ-ment

25

: 591–600.Pigliucci M. (1997) Ontogenetic phenotypic plasticity during the

reproductive phase in

Arabidopsis thaliana

(Brassicaceae).

American Journal of Botany

84

: 887–895.Pigliucci M. (1998) Developmental phenotypic plasticity: where

internal programming meets the external environment.

Current Topics in Plant Biology

1

: 87–91.Pigliucci M. & Schlichting C.D. (1995) Ontogenetic reaction

norms in

Lobelia siphilitica

(Lobeliaceae): response to shading.

Ecology

76

: 2134–2144.Roach D.A. & Wulff R.D. (1987) Maternal effects in plants.

AnnualReview of Ecology and Systematics

18

: 209–235.Sachs T. (2002) Consequences of the inherent developmental

plasticity of organ and tissue relations.

Evolutionary Ecology

16

: 243–265.Schaal B.A. & Leverich J. (1984) Age-specific fitness components

in plants: genotype and phenotype. In:

Population Biology andEvolution

(ed. Loeschcke V.), pp. 173–182. Springer-Verlag,Berlin.

Scheiner S.M. (1993) Genetics and evolution of phenotypic plas-ticity.

Annual Review of Ecology and Systematics

24

: 35–68.Schlichting C.D. (1986) The evolution of phenotypic plasticity in

plants.

Annual Review of Ecology and Systematics

17

: 667–693.Schlichting C.D. & Smith H. (2002) Phenotypic plasticity: linking

molecular mechanisms with evolutionary outcomes.

Evolu-tionary Ecology

16

: 189–211.Schmid B. & Dolt C (1994) Effects of maternal and paternal envi-

ronment and genotype on offspring phenotype in

Solidagoaltissima

L.

Evolution

48

: 1525–1549.Schmitt J. (1995) Genotype–environment interaction, parental

effects, and the evolution of plant reproductive traits. In:

Experimental and Molecular Approaches to Plant Biosystematics

(eds Hoch P. & Stephenson A.G.), pp. 1–16. Missouri Botan-ical Gardens, St. Louis, MO.

Schmitt J., McCormac AC. & Smith H. (1995) A test of the adap-tive plasticity hypothesis using transgenic and mutant plantsdisabled in phytochrome-mediated elongation responses toneighbors.

American Naturalist

146

: 937–953.Shapiro A.M. (1976) Seasonal polyphenism.

Evolutionary Biology

9

: 259–333.Sills G.R. & Nienhuis J. (1995) Maternal phenotypic effects due

to soil nutrient levels and sink removal in

Arabidopsis thaliana

.

American Journal of Botany 82: 491–495.Smith-Gill S.J. (1983) Developmental plasticity: developmental

conversion versus phenotypic modulation. American Zoologist23: 47–55.

Stearns S.C. (1989) The evolutionary significance of phenotypicplasticity. Bioscience 39: 436–445.

Stephenson A.G., Devlin B. & Horton J.B. (1988) The effects ofseed number and prior fruit dominance on the pattern of fruitproduction in Cucurbita pepo (zucchini squash). Annals of Bot-any 62: 653–661.

Stuefer J.F., De Kroon H. & During H.J. (1996) Exploitation ofenvironmental heterogeneity by spatial division of labor in aclonal plant. Functional Ecology 10: 328–344.

Sultan S.E. (1987) Evolutionary implications of phenotypic plas-ticity in plants. Evolutionary Biology 21: 127–178.

Sultan S.E. (1996) Phenotypic plasticity for offspring traits inPolygonum persicaria. Ecology 77: 1791–1807.

Tucic B., Tomic V., Avramov S. & Pemac D. (1998) Testing theadaptive plasticity of Iris pumila leaf traits to natural lightconditions using phenotypic selection analysis. Acta Oecologia19: 473–481.

Van Dam N.M. & Baldwin I.T. (2001) Competition mediates costsof jasmonate-induced defenses, nitrogen acquisition andtransgenerational plasticity in Nicotiana attenuata. FunctionalEcology 15: 406–415.

Van Kleunen M. & Fischer M. (2001) Adaptive evolution ofplastic foraging responses in a clonal plant. Ecology 82: 3309–3319.

Via S., Gomulkiewicz R., de Jong G., Scheiner S.M., SchlichtingC.D. & van Tienderen P.H. (1995) Adaptive phenotypicplasticity: consensus and controversy. Trends in Ecology andEvolution 10: 212–216.

Vogler D.W., Das C. & Stephenson A.G. (1998) Phenotypic plas-ticity in the expression of self-incompatibility in Campanularapunculoides. Heredity 81: 546–555.

Wahl S., Ryser P. & Edwards P.J. (2001) Phenotypic plasticity ofgrass root anatomy in response to light intensity and nutrientsupply. Annals of Botany 88: 1071–1078.

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© 2002 The Society for the Study of Species Biology Plant Species Biology, 17, 85–88

Weinig C. (2000) Plasticity versus canalization: population differ-ences in the timing of shade-avoidance responses. Evolution54: 441–451.

Weinig C. (2002) Phytochrome photoreceptors mediate plasticityto light quality in flowers of the Brassicaceae. American Journalof Botany 89: 230–235.

West-Eberhard M.J. (1989) Phenotypic plasticity and the originsof diversity. Annual Review of Ecology and Systematics 20: 249–278.

Winn A.A. (1999) Is seasonal variation in leaf traits adaptive forthe annual plant Dicerandra linearifolia? Journal of EvolutionaryBiology 13: 306–313.